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Cranial Ontogenetic Variation in Early Saurischians and the Role of Heterochrony in the Diversification of Predatory Dinosaurs Christian Foth1,2,3, Brandon P

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Cranial Ontogenetic Variation in Early Saurischians and the Role of Heterochrony in the Diversification of Predatory Dinosaurs Christian Foth1,2,3, Brandon P Cranial ontogenetic variation in early saurischians and the role of heterochrony in the diversification of predatory dinosaurs Christian Foth1,2,3, Brandon P. Hedrick4,5 and Martin D. Ezcurra2,6,7 1 SNSB, Bayerische Staatssammlung für Paläontologie und Geologie, München, Germany 2 Department of Earth and Environmental Sciences, Ludwig-Maximilians-Universität, München, Germany 3 Department of Geosciences, University of Fribourg/Freiburg, Fribourg, Switzerland 4 Department of Earth and Environmental Science, University of Pennsylvania, Philadelphia, PA, United States 5 Department of Biology, University of Massachusetts, Amherst, MA, United States 6 CONICET, Sección Paleontología de Vertebrados, Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina 7 School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, United Kingdom ABSTRACT Non-avian saurischian skulls underwent at least 165 million years of evolution and shapes varied from elongated skulls, such as in the theropod Coelophysis, to short and box-shaped skulls, such as in the sauropod Camarasaurus. A number of factors have long been considered to drive skull shape, including phylogeny, dietary preferences and functional constraints. However, heterochrony is increasingly being recognized as an important factor in dinosaur evolution. In order to quantitatively analyse the impact of heterochrony on saurischian skull shape, we analysed five ontogenetic trajectories using two-dimensional geometric morphometrics in a phylogenetic framework. This allowed for the comparative investigation of main ontogenetic shape changes and the evaluation of how heterochrony affected skull shape through both ontogenetic and phylogenetic trajectories. Using principal component analyses and multivariate regressions, it was possible to quantify different ontogenetic trajectories and evaluate Submitted 17 June 2015 them for evidence of heterochronic events allowing testing of previous hypotheses on Accepted 21 December 2015 Published 18 January 2016 cranial heterochrony in saurischians. We found that the skull shape of the hypothetical ancestor of Saurischia likely led to basal Sauropodomorpha through paedomorphosis, Corresponding author Christian Foth, chris- and to basal Theropoda mainly through peramorphosis. Paedomorphosis then led [email protected] from Orionides to Avetheropoda, indicating that the paedomorphic trend found by Academic editor previous authors in advanced coelurosaurs may extend back into the early evolution of Jesús Marugán-Lobón Avetheropoda. Not only are changes in saurischian skull shape complex due to the large Additional Information and number of factors that affected it, but heterochrony itself is complex, with a number of Declarations can be found on possible reversals throughout non-avian saurischian evolution. In general, the sampling page 28 of complete ontogenetic trajectories including early juveniles is considerably lower than DOI 10.7717/peerj.1589 the sampling of single adult or subadult individuals, which is a major impediment to the study of heterochrony on non-avian dinosaurs. Thus, the current work represents Copyright 2016 Foth et al. an exploratory analysis. To better understand the cranial ontogeny and the impact of heterochrony on skull evolution in saurischians, the data set that we present here must Distributed under be expanded and complemented with further sampling from future fossil discoveries, Creative Commons CC-BY 4.0 especially of juvenile individuals. OPEN ACCESS How to cite this article Foth et al. (2016), Cranial ontogenetic variation in early saurischians and the role of heterochrony in the diversifi- cation of predatory dinosaurs. PeerJ 4:e1589; DOI 10.7717/peerj.1589 Subjects Biodiversity, Evolutionary Studies, Paleontology, Taxonomy, Zoology Keywords Ontogeny, Sauropodomorpha, Evolution, Theropoda, Skull shape, Dinosauria, Heterochrony, Geometric morphometrics INTRODUCTION In an evolutionary context, heterochrony describes phenotypic changes due to shifts in the timing or rate of developmental processes in an organism relative to its ancestor, and can lead to significant evolutionary changes in body plans within relatively short periods of time (Gould, 1977; Alberch et al., 1979; McNamara, 1982; Reilly, Wiley & Meinhardt, 1997; Klingenberg, 1998; McNamara & McKinney, 2005). Two major types of heterochronic processes are discerned: paedomorphosis and peramorphosis. Paedo- morphosis occurs when the later ontogenetic stages of an organism retain characteristics from earlier ontogenetic stages of its ancestor due to a truncation of the growth period (progenesis), decrease of the growth rate (neoteny) or a delayed onset of developmental processes (postdisplacement). In contrast, a peramorphic organism is ontogenetically more developed than the later ontogenetic stages of its ancestor due to the extension of growth period (hypermorphosis), the increase of the growth rate (acceleration) or the earlier onset of developmental processes (predisplacement) (see Gould, 1977; Alberch et al., 1979; Klingenberg, 1998). In practice, evidence for heterochronic events in evolution can be detected by comparing the ontogenetic trajectories of different taxa under the consideration of their phylogenetic interrelationships (Alberch et al., 1979; Fink, 1982). Thus, the concept of heterochrony connects two main fields of biological sciences: developmental and evolutionary biology (Gould, 1977; Raff, 1996). When studying heterochrony, ontogenetic trajectories are characterized by three separate vectors (size, shape, and ontogenetic age), which allows for quantification of heterochronic processes with slope, length and position within a Euclidean space (Alberch et al., 1979). In this context, geometric morphometrics is a useful method for characterizing shape and size vectors to investigate heterochrony in organisms within a multivariate framework (Mitteroecker, Gunz & Bookstein, 2005). Documentation of heterochrony in the vertebrate fossil record is limited. Preserved fossil ontogenetic series covering the whole postnatal development of fossil species are rare due to the fact that early juvenile specimens are often either lacking or incomplete. Furthermore, exact ages of single ontogenetic stages are often not available, resulting in the temporal component often being replaced by size, which is not an ideal variable for age (Klingenberg, 1998; Gould, 2000). Nevertheless, the role of heterochrony has been recognized and discussed for the evolution of multiple fossil lineages that do preserve ontogenetic series (Balanoff & Rowe, 2007; Gerber, Neige & Eble, 2007; Schoch, 2009; Schoch, 2010; Schoch, 2014; Bhullar, 2012; Forasiepi & Sánchez-Villagra, 2014; Ezcurra & Butler, 2015), including non-avian dinosaurs (e.g., Long & McNamara, 1997; Erickson et al., 2004; Guenther, 2009; Bhullar et al., 2012; Canale et al., 2014). For example, Long & McNamara (1997), Erickson et al. (2004) and Canale et al. (2014) hypothesized that the evolution of large body size in carcharodontosaurids and tyrannosaurids from medium-sized ancestors was the result of peramorphosis. Foth et al. (2016), PeerJ, DOI 10.7717/peerj.1589 2/41 There has recently been an increasing interest in shape diversity in non-avian dinosaurs, in which geometric morphometric methods have been applied on a regular basis (e.g., Bonnan, 2004; Chinnery, 2004; Campione & Evans, 2011; Hedrick & Dodson, 2013; Lautenschlager, 2014; Schwarz-Wings & Böhm, 2014; Maiorini et al., 2015). Skull shape diversity in saurischian dinosaurs has been studied in particular detail (e.g., Henderson, 2002; Young & Larvan, 2010; Rauhut et al., 2011; Brusatte et al., 2012; Bhullar et al., 2012; Foth & Rauhut, 2013a; Foth & Rauhut, 2013b), but usually in relation to functional constraints, dietary preferences, phylogenetic interrelationships, and macroevolutionary patterns. For example, these studies have shown that skull shape in sauropodomorphs and theropods is phylogenetically constrained (Young & Larvan, 2010; Brusatte et al., 2012; Foth & Rauhut, 2013a) and that the shape of the orbit in theropods is functionally constrained (Henderson, 2002; Foth & Rauhut, 2013a). Thus, geometric morphometrics is a powerful method to quantify both intraspecific (e.g., ontogeny, sexual dimorphism, polymorphism) and interspecific (e.g., systematics, macroevolution) shape variation on the basis of homologous landmarks or outlines, which capture more information about shape than traditional morphometric measurements (Corti, 1993; Rohlf & Marcus, 1993; Adams, Rohlf & Slice, 2004; Adams, Rohlf & Slice, 2013; Slice, 2007; Mitteroecker & Gunz, 2009; Zelditch, Swiderski & Sheets, 2012). As a result, geometric morphometrics has also been successfully applied to the study of heterochrony among various tetrapod groups, in which the univariate mathematical approach of Alberch et al. (1979) was adapted to a multivariate framework (e.g., Berge & Penin, 2004; Mitteroecker et al., 2004; Mitteroecker, Gunz & Bookstein, 2005; Lieberman et al., 2007; Drake, 2011; Piras et al., 2011; Bhullar et al., 2012). However, only Bhullar et al. (2012) have examined cranial shape diversity of theropod dinosaurs using multivariate methods in the context of heterochrony. This pioneering study demonstrated that recent birds have highly paedomorphic skulls compared to non-avian theropods and Mesozoic birds (e.g., Archaeopteryx and Enantiornithes), which evolved in a multistep transformation within the clade Eumaniraptora. Furthermore, Bhullar
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